Socially cued anticipatory adjustment of female signalling effort in a moth.

Juvenile population density has profound effects on subsequent adult development, morphology and reproductive investment. Yet, little is known about how the juvenile social environment affects adult investment into chemical sexual signalling. Male gumleaf skeletonizer moths, Uraba lugens, facultatively increase investment into antennae (pheromone receiving structures) when reared at low juvenile population densities, but whether there is comparable adjustment by females into pheromone investment is not known. We investigate how juvenile population density influences the 'calling' (pheromone-releasing) behaviour of females and the attractiveness of their pheromones. Female U. lugens adjust their calling behaviour in response to socio-sexual cues: adult females reared in high juvenile population densities called earlier and for longer than those from low juvenile densities. Juvenile density also affected female pheromonal attractiveness: Y-maze olfactometer assays revealed that males prefer pheromones produced by females reared at high juvenile densities. This strategic investment in calling behaviour by females, based on juvenile cues that anticipate the future socio-sexual environment, likely reflects a response to avoid mating failure through competition with neighbouring signallers.

Territoriality in ants revisited: iconic collective displays reflect resource, not territorial defense in meat ants Iridomyrmex purpureus.

Non-injurious, collective ritualized displays may have evolved in some species of ants as a means of resolving contests for key resources, without causing a drain in worker numbers through injury. Colonies of the Australian meat ant, Iridomyrmex purpureus, deploy numerous workers to engage in collective displays, which are widely understood to be involved in maintaining exclusive territories. A combination of field surveys and behavioral assays revealed that display grounds do not delimit borders that define exclusive territories. Rather, the proportion of workers from a focal colony found in a quadrat declines monotonically with distance from the nest. In addition, we documented collective displays around food trees, where workers congregated in greater densities and engaged in more aggressive behavior. These results refute the assumption that colonies of I. purpureus establish territorial boundaries by collective displays. Rather these collective displays may be related to the defense of specific resources, including food trees and nest sites. The difference in the level of aggression among displaying workers at different locations may reflect a balance between the benefits of defending a particular resource and an unappreciated cost of escalation.

Solitary bees reduce investment in communication compared with their social relatives.

Social animals must communicate to define group membership and coordinate social organization. For social insects, communication is predominantly mediated through chemical signals, and as social complexity increases, so does the requirement for a greater diversity of signals. This relationship is particularly true for advanced eusocial insects, including ants, bees, and wasps, whose chemical communication systems have been well-characterized. However, we know surprisingly little about how these communication systems evolve during the transition between solitary and group living. Here, we demonstrate that the sensory systems associated with signal perception are evolutionarily labile. In particular, we show that differences in signal production and perception are tightly associated with changes in social behavior in halictid bees. Our results suggest that social species require a greater investment in communication than their solitary counterparts and that species that have reverted from eusociality to solitary living have repeatedly reduced investment in these potentially costly sensory perception systems.

Antennal scales improve signal detection efficiency in moths.

The elaborate bipectinate antennae of male moths are thought to increase their sensitivity to female sex pheromones, and so should be favoured by selection. Yet simple filamentous antennae are the most common structure among moths. The stereotypic arrangements of scales on the surface of antennae may resolve this paradox. We use computational fluid dynamics techniques to model how scales on the filamentous antennae of moths affect the passage of different particles in the airflow across the flagellum in both small and large moths. We found that the scales provide an effective solution to improve the efficacy of filamentous antennae, by increasing the concentration of nanoparticles, which resemble pheromones, around the antennae. The smaller moths have a greater increase in antennal efficiency than larger moths. The scales also divert microparticles, which resemble dust, away from the antennal surface, thereby reducing contamination. The positive correlations between antennal scale angles and sensilla number across Heliozelidae moths are consistent with the predictions of our model.

Insect Antennal Morphology: The Evolution of Diverse Solutions to Odorant Perception.

Chemical communication involves the production, transmission, and perception of odors. Most adult insects rely on chemical signals and cues to locate food resources, oviposition sites or reproductive partners and, consequently, numerous odors provide a vital source of information. Insects detect these odors with receptors mostly located on the antennae, and the diverse shapes and sizes of these antennae (and sensilla) are both astonishing and puzzling: what selective pressures are responsible for these different solutions to the same problem - to perceive signals and cues? This review describes the selection pressures derived from chemical communication that are responsible for shaping the diversity of insect antennal morphology. In particular, we highlight new technologies and techniques that offer exciting opportunities for addressing this surprisingly neglected and yet crucial component of chemical communication.

Anticipatory flexibility: larval population density in moths determines male investment in antennae, wings and testes.

Developmental plasticity provides individuals with a distinct advantage when the reproductive environment changes dramatically. Variation in population density, in particular, can have profound effects on male reproductive success. Females may be easier to locate in dense populations, but there may be a greater risk of sperm competition. Thus, males should invest in traits that enhance fertilization success over traits that enhance mate location. Conversely, males in less dense populations should invest more in structures that will facilitate mate location. In Lepidoptera, this may result in the development of larger antennae to increase the likelihood of detecting female sex pheromones, and larger wings to fly more efficiently. We explored the effects of larval density on adult morphology in the gum-leaf skeletonizer moth, Uraba lugens, by manipulating both the number of larvae and the size of the rearing container. This experimental arrangement allowed us to reveal the cues used by larvae to assess whether absolute number or density influences adult responses. Male investment in testes size depended on the number of individuals, while male investment in wings and antennae depended upon larval density. By contrast, the size of female antennae and wings were influenced by an interaction of larval number and container size. This study demonstrates that male larvae are sensitive to cues that may reveal adult population density, and adjust investment in traits associated with fertilization success and mate detection accordingly.

Sexual selection on receptor organ traits: younger females attract males with longer antennae.

Sexual selection theory predicts that female choice may favour the evolution of elaborate male signals. Darwin also suggested that sexual selection can favour elaborate receiver structures in order to better detect sexual signals, an idea that has been largely ignored. We evaluated this unorthodox perspective by documenting the antennal lengths of male Uraba lugens Walker (Lepidoptera: Nolidae) moths that were attracted to experimentally manipulated emissions of female sex pheromone. Either one or two females were placed in field traps for the duration of their adult lives in order to create differences in the quantity of pheromone emissions from the traps. The mean antennal length of males attracted to field traps baited with a single female was longer than that of males attracted to traps baited with two females, a pattern consistent with Darwin's prediction assuming the latter emits higher pheromone concentrations. Furthermore, younger females attracted males with longer antennae, which may reflect age-specific changes in pheromone emission. These field experiments provide the first direct evidence of an unappreciated role for sexual selection in the evolution of sexual dimorphism in moth antennae and raise the intriguing possibility that females select males with longer antennae through strategic emission of pheromones.

The evolution of genital complexity and mating rates in sexually size dimorphic spiders.

BACKGROUND: Genital diversity may arise through sexual conflict over polyandry, where male genital features function to manipulate female mating frequency against her interest. Correlated genital evolution across animal groups is consistent with this view, but a link between genital complexity and mating rates remains to be established. In sexually size dimorphic spiders, golden orbweaving spiders (Nephilidae) males mutilate their genitals to form genital plugs, but these plugs do not always prevent female polyandry. In a comparative framework, we test whether male and female genital complexity coevolve, and how these morphologies, as well as sexual cannibalism, relate to the evolution of mating systems. RESULTS: Using a combination of comparative tests, we show that male genital complexity negatively correlates with female mating rates, and that levels of sexual cannibalism negatively correlate with male mating rates. We also confirm a positive correlation between male and female genital complexity. The macroevolutionary trajectory is consistent with a repeated evolution from polyandry to monandry coinciding with the evolution towards more complex male genitals. CONCLUSIONS: These results are consistent with the predictions from sexual conflict theory, although sexual conflict may not be the only mechanism responsible for the evolution of genital complexity and mating systems. Nevertheless, our comparative evidence suggests that in golden orbweavers, male genital complexity limits female mating rates, and sexual cannibalism by females coincides with monogyny.

Location-specific cuticular hydrocarbon signals in a social insect.

Social insects use cuticular hydrocarbons (CHCs) to convey different social signals, including colony or nest identity. Despite extensive investigations, the exact source and identity of CHCs that act as nest-specific identification signals remain largely unknown. Perhaps this is because studies that identify CHC signals typically use organic solvents to extract a single sample from the entire animal, thereby analysing a cocktail of chemicals that may serve several signal functions. We took a novel approach by first identifying CHC profiles from different body parts of ants (Iridomyrmex purpureus), then used behavioural bioassays to reveal the location of specific social signals. The CHC profiles of both workers and alates varied between different body parts, and workers paid more attention to the antennae of non-nest-mate and the legs of nest-mate workers. Workers responded less aggressively to non-nest-mate workers if the CHCs on the antennae of their opponents were removed with a solvent. These data indicate that CHCs located on the antennae reveal nest-mate identity and, remarkably, that antennae both convey and receive social signals. Our approach and findings could be valuably applied to chemical signalling in other behavioural contexts, and provide insights that were otherwise obscured by including chemicals that either have no signal function or may be used in other contexts.

Signal polymorphism under a constant environment: the odd cross in a web decorating spider.

The quality of many animal signals varies, perhaps through their use in different contexts or by representing an adaptive response to reduce the risk of exploitation. Spiders of the orb weaver genus Argiope add linear, cruciate or circular silk structures to their orb webs, creating inter- and intra-specific polymorphic visual signals. Different decoration patterns are frequently attributed to different signal effects, but this view is contradicted by commonly observed intraspecific variation in decorating behaviour. Adults of Argiope mascordi are bimodal web decorators, building two distinct patterns, circular and cruciate silk structures. We investigated the variation of patterns under controlled, invariant laboratory conditions. Circular decorations were most frequent, but individuals often switch to the other pattern. This variation neither increased nor decreased over time, suggesting that pattern variability is primarily intrinsic rather than an exclusive response to environmental changes. Accordingly, we discuss the evolutionary implications in the light of the conservation of a single signal function through maintaining the variation of its quality and the alternative view that silk decorations may not represent adaptive signals at all.

Eavesdropping on cooperative communication within an ant-butterfly mutualism.

Signalling is necessary for the maintenance of interspecific mutualisms but is vulnerable to exploitation by eavesdropping. While eavesdropping of intraspecific signals has been studied extensively, such exploitation of interspecific signals has not been widely documented. The juvenile stages of the Australian lycaenid butterfly, Jalmenus evagoras, form an obligate association with several species of attendant ants, including Iridomyrmex mayri. Ants protect the caterpillars and pupae, and in return are rewarded with nutritious secretions. Female and male adult butterflies use ants as signals for oviposition and mate searching, respectively. Our experiments reveal that two natural enemies of J. evagoras, araneid spiders and braconid parasitoid wasps, exploit ant signals as cues for increasing their foraging and oviposition success, respectively. Intriguingly, selection through eavesdropping is unlikely to modify the ant signal.

Ecological specialisation in habitat selection within a macropodid herbivore guild.

Specialist species show stronger resource selection, narrower niches and lower niche overlap than generalist species. We examined ecological specialisation with respect to habitat selection in a macropodid community comprising the western grey kangaroo Macropus fuliginosus, red-necked wallaby M. rufogriseus and swamp wallaby Wallabia bicolor in the Grampians National Park, Victoria, Australia. We used radio tracking to quantify habitat selection. We predicted that because the fitness benefits of generalisation and specialisation differ, there would be a mix of generalised and specialised species in our community. As all three macropodid species show marked sexual dimorphism, we also expected that they would show sex-based specialisation. Finally, because many large herbivores select different habitats for foraging and resting, we predicted that our species would specialise on a subset of their overall selected habitat based on activity period (diurnal or nocturnal). All three species specialised on the available resources to some degree. Western grey kangaroos were specialists, at least during the active period. Niche data for the two wallaby species were harder to interpret so we could not determine their degree of specialisation. Within species, we found no evidence of sex-based specialisation. However, we found clear evidence of specialisation by activity period in western grey kangaroos and red-necked wallabies, but not in swamp wallabies. The strength of behavioural decisions made during the active period in influencing specialisation points to the likelihood that bottom-up processes regulate this community.

Parasite and predator risk assessment: nuanced use of olfactory cues.

Foraging herbivores face twin threats of predation and parasite infection, but the risk of predation has received much more attention. We evaluated, experimentally, the role of olfactory cues in predator and parasite risk assessment on the foraging behaviour of a population of marked, free-ranging, red-necked wallabies (Macropus rufogriseus). The wallabies adjusted their behaviour according to these olfactory cues. They foraged less, were more vigilant and spent less time at feeders placed in the vicinity of faeces from dogs that had consumed wallaby or kangaroo meat compared with that of dogs feeding on sheep, rabbit or possum meat. Wallabies also showed a species-specific faecal aversion by consuming less food from feeders contaminated with wallaby faeces compared with sympatric kangaroo faeces, whose gastrointestinal parasite fauna differs from that of the wallabies. Combining both parasite and predation cues in a single field experiment revealed that these risks had an additive effect, rather than the wallabies compromising their response to one risk at the expense of the other.

Females adopt sexual catalepsy to facilitate mating.

Theory predicts that males and females of dioecious species typically engage in an evolutionary sexual conflict over the frequency and choice of mating partner. Female sexual cannibalism, a particularly dramatic illustration of this conflict, is widespread in certain animal taxa including spiders. Nevertheless, females of some funnel weaving spiders that are generally aggressive to conspecifics enter a cataleptic state after male courtship, ensuring the males can mate without risk of attack. In this study, we demonstrated that the physical posture and duration, metabolites, and central neurotransmitters of females of Aterigena aculeata in sexual catalepsy closely resemble females in thanatosis but are distinct from those in anesthesia, indicating that the courted females feign death to eliminate the risk of potentially aggressive responses and thereby allow preferred males to mate. Unlike the taxonomically widespread thanatosis, which generally represents a deceptive visual signal that acts against the interest of the receivers, sexual catalepsy of females in the funnel weaving spiders may deliver a sexual-receptive signal to the courting males and thereby benefit both the signal senders and receivers. Therefore, sexual catalepsy in A. aculeata may not reflect a conflict but rather a confluence of interest between the sexes.

Density of antennal sensilla influences efficacy of communication in a social insect.

Effective communication requires reliable signals and competent receptors. Theoretical and empirical accounts of animal signaling focus overwhelmingly on the capacity of the signaler to convey the message. Nevertheless, the intended receiver's ability to detect a signal depends on the condition of its receptor organs, as documented for humans. The impact of receptor organ condition on signal reception and its consequences for functional behavior are poorly understood. Social insects use antennae to detect chemical odors that distinguish between nestmates and enemies, reacting aggressively to the latter. We investigated the impact of antennal condition, determined by the density of sensilla, on the behavior of the weaver ant Oecophylla smaragdina. Worker aggression depended upon the condition of their antennae: workers with fewer sensilla on their antennae reacted less aggressively to nonnestmate enemies. These novel data highlight the largely unappreciated significance of receptor organ condition for animal communication and may have implications for coevolutionary processes in animal communication.

Promiscuous words.

Promiscuity is frequently used to describe animal mating behaviour, and especially to describe multiple mating by females. Yet this use of the term is incorrect, perhaps reflecting an erroneous adoption of common language to pique reader interest. We evaluated the patterns of use and misuse of the word 'promiscuity' in a representative journal of animal behaviour. This survey highlights how inappropriately the term is used, and how it can conceal critical features of animal mating strategies with intriguing evolutionary significance. Further analysis of the scientific impact of papers identified by the term promiscuous or polyandrous revealed that the former were cited less frequently. We argue that using promiscuity to describe animal mating strategies is anthropomorphic, inaccurate, and potentially misleading. Consistent with other biological disciplines, the word promiscuity should be used to describe indiscriminate mating behaviour only, and that polygyny and polyandry should be used to describe male and female mating frequency respectively.

Colony-level aggression escalates with the value of food resources.

BACKGROUND: Theory predicts that the level of escalation in animal contests is associated with the value of the contested resource. This fundamental prediction has been empirically confirmed by studies of dyadic contests but has not been tested experimentally in the collective context of group-living animals. Here, we used the Australian meat ant Iridomyrmex purpureus as a model and employed a novel field experimental manipulation of the value of food that removes the potentially confounding effects of nutritional status of the competing individual workers. We draw on insights from the Geometric Framework for nutrition to investigate whether group contests between neighbouring colonies escalate according to the value to the colony of a contested food resource. RESULTS: First, we show that colonies of I. purpureus value protein according to their past nutritional intake, deploying more foragers to collect protein if their previous diet had been supplemented with carbohydrate rather than with protein. Using this insight, we show that colonies contesting more highly valued food escalated the contest, by deploying more workers and engaging in lethal 'grappling' behaviour. CONCLUSION: Our data confirm that a key prediction of contest theory, initially intended for dyadic contests, is similarly applicable to group contests. Specifically, we demonstrate, through a novel experimental procedure, that the contest behaviour of individual workers reflects the nutritional requirements of the colony, rather than that of individual workers.

Short-term particulate matter contamination severely compromises insect antennal olfactory perception.

The consequences of sub-lethal levels of ambient air pollution are underestimated for insects, for example, the accumulation of particulate matter on sensory receptors located on their antennae may have detrimental effects to their function. Here we show that the density of particulate matter on the antennae of houseflies (Musca domestica) collected from an urban environment increases with the severity of air pollution. A combination of behavioural assays, electroantennograms and transcriptomic analysis provide consistent evidence that a brief exposure to particulate matter pollution compromises olfactory perception of reproductive and food odours in both male and female houseflies. Since particulate matter can be transported thousands of kilometres from its origin, these effects may represent an additional factor responsible for global declines in insect numbers, even in pristine and remote areas.

A novel property of spider silk: chemical defence against ants.

Spider webs are made of silk, the properties of which ensure remarkable efficiency at capturing prey. However, remaining on, or near, the web exposes the resident spiders to many potential predators, such as ants. Surprisingly, ants are rarely reported foraging on the webs of orb-weaving spiders, despite the formidable capacity of ants to subdue prey and repel enemies, the diversity and abundance of orb-web spiders, and the nutritional value of the web and resident spider. We explain this paradox by reporting a novel property of the silk produced by the orb-web spider Nephila antipodiana (Walckenaer). These spiders deposit on the silk a pyrrolidine alkaloid (2-pyrrolidinone) that provides protection from ant invasion. Furthermore, the ontogenetic change in the production of 2-pyrrolidinone suggests that this compound represents an adaptive response to the threat of natural enemies, rather than a simple by-product of silk synthesis: while 2-pyrrolidinone occurs on the silk threads produced by adult and large juvenile spiders, it is absent on threads produced by small juvenile spiders, whose threads are sufficiently thin to be inaccessible to ants.